Skip to main content

Advertisement

SpringerLink
Log in

High prevalence of mec complex C and ccrC is independent of SCCmec type V in Staphylococcus haemolyticus

  • Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

Staphylococcus haemolyticus is one of the most clinically relevant coagulase-negative staphylococci (CoNS), particularly in immunocompromised patients; however, little is known regarding its molecular epidemiology. In this work, we characterized the genetic background and the SCCmec region of 36 methicillin-resistant S. haemolyticus (MRSHae) and 10 methicillin-susceptible S. haemolyticus (MSSHae) collected from neutropenic patients in Tunisia between 2002 and 2004. The molecular characterization of MRSHae by pulsed-field gel electrophoresis (PFGE) showed that the great majority of the isolates (77.8%) belonged to only four types. SCCmec typing by polymerase chain reaction (PCR) and Southern hybridization showed that isolates belonging to each PFGE type could carry either one or two SCCmec types. SCCmec V was the most common, but mec complex C was frequently associated to ccr allotypes other than ccrC. The mec complex class C was predominant in MRSHae (47%) and ccrC was predominant among both methicillin-resistant and -susceptible isolates (31 and 50%, respectively). Interestingly, one half (50%) of the MRSHae isolates analyzed lacked the known ccr complexes (ccrAB and ccrC), although they carried the mecA. Conversely, all MSSHae carrying a ccrC complex were multidrug-resistant, although they lack the mecA. The results suggest that ccrC and mec complex C are frequent and may exist autonomously and independently of SCCmec type V in S. haemolyticus. Moreover, the data obtained suggest that small chromosomal rearrangements promoting the loss or structural variation of mec and ccr complex appear to occur frequently, which probably provide S. haemolyticus with a specialized means for SCCmec trapping and/or diversification.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Tabe Y, Nakamura A, Oguri T, Igari J (1998) Molecular characterization of epidemic multiresistant Staphylococcus haemolyticus isolates. Diagn Microbiol Infect Dis 32:177–183

    Article  PubMed  CAS  Google Scholar 

  2. Campanile F, Bongiorno D, Borbone S, Falcone M, Giannella M, Venditti M et al (2008) In vitro activity of daptomycin against methicillin- and multi-resistant Staphylococcus haemolyticus invasive isolates carrying different mec complexes. Diagn Microbiol Infect Dis 61:227–231

    Article  PubMed  CAS  Google Scholar 

  3. Mombach Pinheiro Machado AB, Reiter KC, Paiva RM, Barth AL (2007) Distribution of staphylococcal cassette chromosome mec (SCCmec) types I, II, III and IV in coagulase-negative staphylococci from patients attending a tertiary hospital in southern Brazil. J Med Microbiol 56:1328–1333

    Article  PubMed  CAS  Google Scholar 

  4. Kloos WE, Bannerman TL (1995) Staphylococcus and Micrococcus. In: Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH (eds) Manual of clinical microbiology. ASM Press, Washington, pp 282–298

    Google Scholar 

  5. Takeuchi F, Watanabe S, Baba T, Yuzawa H, Ito T, Morimoto Y et al (2005) Whole-genome sequencing of Staphylococcus haemolyticus uncovers the extreme plasticity of its genome and the evolution of human-colonizing staphylococcal species. J Bacteriol 187:7292–7308

    Article  PubMed  CAS  Google Scholar 

  6. Santos Sanches I, Mato R, de Lencastre H, Tomasz A, CEM/NET Collaborators and the International Collaborators (2000) Patterns of multidrug resistance among methicillin-resistant hospital isolates of coagulase-positive and coagulase-negative staphylococci collected in the international multicenter study RESIST in 1997 and 1998. Microb Drug Resist 6:199–211

    Article  PubMed  CAS  Google Scholar 

  7. Yu MH, Chen YG, Yu YS, Chen CL, Li LJ (2010) Antimicrobial resistance and molecular characterization of Staphylococcus haemolyticus in a Chinese hospital. Eur J Clin Microbiol Infect Dis 29:613–616

    Article  PubMed  CAS  Google Scholar 

  8. Hartman BJ, Tomasz A (1984) Low-affinity penicillin-binding protein associated with β-lactam resistance in Staphylococcus aureus. J Bacteriol 158:513–516

    PubMed  CAS  Google Scholar 

  9. Katayama Y, Ito T, Hiramatsu K (2000) A new class of genetic element, staphylococcus cassette chromosome mec, encodes methicillin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 44:1549–1555

    Article  PubMed  CAS  Google Scholar 

  10. Ito T, Katayama Y, Hiramatsu K (1999) Cloning and nucleotide sequence determination of the entire mec DNA of pre-methicillin-resistant Staphylococcus aureus N315. Antimicrob Agents Chemother 43:1449–1458

    PubMed  CAS  Google Scholar 

  11. Ito T, Ma XX, Takeuchi F, Okuma K, Yuzawa H, Hiramatsu K (2004) Novel type V staphylococcal cassette chromosome mec driven by a novel cassette chromosome recombinase, ccrC. Antimicrob Agents Chemother 48:2637–2651

    Article  PubMed  CAS  Google Scholar 

  12. International Working Group on the Classification of Staphylococcal Cassette Chromosome Elements (IWG-SCC) (2009) Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements. Antimicrob Agents Chemother 53:4961–4967

    Article  Google Scholar 

  13. Ito T, Katayama Y, Asada K, Mori N, Tsutsumimoto K, Tiensasitorn C et al (2001) Structural comparison of three types of staphylococcal cassette chromosome mec integrated in the chromosome in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 45:1323–1336

    Article  PubMed  CAS  Google Scholar 

  14. Ito T, Okuma K, Ma XX, Yuzawa H, Hiramatsu K (2003) Insights on antibiotic resistance of Staphylococcus aureus from its whole genome: genomic island SCC. Drug Resist Updat 6:41–52

    Article  PubMed  CAS  Google Scholar 

  15. Ma XX, Ito T, Tiensasitorn C, Jamklang M, Chongtrakool P, Boyle-Vavra S et al (2002) Novel type of staphylococcal cassette chromosome mec identified in community-acquired methicillin-resistant Staphylococcus aureus strains. Antimicrob Agents Chemother 46:1147–1152

    Article  PubMed  CAS  Google Scholar 

  16. Ruppé E, Barbier F, Mesli Y, Maiga A, Cojocaru R, Benkhalfat M et al (2009) Diversity of staphylococcal cassette chromosome mec structures in methicillin-resistant Staphylococcus epidermidis and Staphylococcus haemolyticus strains among outpatients from four countries. Antimicrob Agents Chemother 53:442–449

    Article  PubMed  Google Scholar 

  17. Nunes APF, Teixeira LM, Bastos CCR, Silva MG, Ferreira RBR, Fonseca LS et al (2005) Genomic characterization of oxacillin-resistant Staphylococcus epidermidis and Staphylococcus haemolyticus isolated from Brazilian medical centres. J Hosp Infect 59:19–26

    Article  PubMed  CAS  Google Scholar 

  18. Couto I, Pereira S, Miragaia M, Sanches IS, de Lencastre H (2001) Identification of clinical staphylococcal isolates from humans by internal transcribed spacer PCR. J Clin Microbiol 39:3099–3103

    Article  PubMed  CAS  Google Scholar 

  19. Ham JS, Lee SG, Jeong SG, Oh MH, Kim DH, Lee T et al (2010) Powerful usage of phylogenetically diverse Staphylococcus aureus control strains for detecting multidrug resistance genes in transcriptomics studies. Mol Cells 30:71–76

    Article  PubMed  CAS  Google Scholar 

  20. Gill SR, Fouts DE, Archer GL, Mongodin EF, Deboy RT, Ravel J et al (2005) Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J Bacteriol 187:2426–2438

    Article  PubMed  CAS  Google Scholar 

  21. Oliveira DC, Milheiriço C, Vinga S, de Lencastre H (2006) Assessment of allelic variation in the ccrAB locus in methicillin-resistant Staphylococcus aureus clones. J Antimicrob Chemother 58:23–30

    Article  PubMed  CAS  Google Scholar 

  22. Oliveira DC, Tomasz A, de Lencastre H (2001) The evolution of pandemic clones of methicillin-resistant Staphylococcus aureus: identification of two ancestral genetic backgrounds and the associated mec elements. Microb Drug Resist 7:349–361

    Article  PubMed  CAS  Google Scholar 

  23. Oliveira DC, Tomasz A, de Lencastre H (2002) Secrets of success of a human pathogen: molecular evolution of pandemic clones of meticillin-resistant Staphylococcus aureus. Lancet Infect Dis 2:180–189

    Article  PubMed  CAS  Google Scholar 

  24. Chongtrakool P, Ito T, Ma XX, Kondo Y, Trakulsomboon S, Tiensasitorn C et al (2006) Staphylococcal cassette chromosome mec (SCCmec) typing of methicillin-resistant Staphylococcus aureus strains isolated in 11 Asian countries: a proposal for a new nomenclature for SCCmec elements. Antimicrob Agents Chemother 50:1001–1012

    Article  PubMed  CAS  Google Scholar 

  25. Okuma K, Iwakawa K, Turnidge JD, Grubb WB, Bell JM, O’Brien FG et al (2002) Dissemination of new methicillin-resistant Staphylococcus aureus clones in the community. J Clin Microbiol 40:4289–4294

    Article  PubMed  CAS  Google Scholar 

  26. Lina G, Etienne J, Vandenesch F (2000) Biology and pathogenicity of staphylococci other than Staphylococcus aureus and Staphylococcus epidermidis. In: Fischitti VA, Novick RP, Ferretti JJ, Portnoy DA, Rood JI (eds) Gram-positive pathogens. ASM Press, Washington, pp 450–462

    Google Scholar 

  27. Chlebowicz MA, Nganou K, Kozytska S, Arends JP, Engelmann S, Grundmann H et al (2010) Recombination between ccrC genes in a type V (5C2&5) staphylococcal cassette chromosome mec (SCCmec) of Staphylococcus aureus ST398 leads to conversion from methicillin resistance to methicillin susceptibility in vivo. Antimicrob Agents Chemother 54:783–791

    Article  PubMed  CAS  Google Scholar 

  28. Oliveira DC, Wu SW, de Lencastre H (2000) Genetic organization of the downstream region of the mecA element in methicillin-resistant Staphylococcus aureus isolates carrying different polymorphisms of this region. Antimicrobial Agents Chemother 44:1906–1910

    Article  CAS  Google Scholar 

  29. Enright MC, Robinson DA, Randle G, Feil EJ, Grundmann H, Spratt BG (2002) The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc Natl Acad Sci USA 99:7687–7692

    Article  PubMed  CAS  Google Scholar 

  30. Kuroda M, Ohta T, Uchiyama I, Baba T, Yuzawa H, Kobayashi I et al (2001) Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357:1225–1240

    Article  PubMed  CAS  Google Scholar 

  31. Hanssen AM, Sollid JU (2007) Multiple staphylococcal cassette chromosomes and allelic variants of cassette chromosome recombinases in Staphylococcus aureus and coagulase-negative staphylococci from Norway. Antimicrob Agents Chemother 51:1671–1677

    Article  PubMed  CAS  Google Scholar 

  32. Bouchami O, Ben Hassen A, de Lencastre H, Miragaia M (2011) Molecular epidemiology of methicillin-resistant Staphylococcus hominis (MRSHo): Low Clonality and Reservoirs of SCCmec Structural Elements. PLoS One 6:e21940

  33. Berglund C, Söderquist B (2008) The origin of a methicillin-resistant Staphylococcus aureus isolate at a neonatal ward in Sweden—possible horizontal transfer of a staphylococcal cassette chromosome mec between methicillin-resistant Staphylococcus haemolyticus and Staphylococcus aureus. Clin Microbiol Infect 14:1048–1056

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the investigators who kindly provided some of the bacterial strains used in the study: K. Hiramatsu and T. Ito for the strains NCTC10442, N315, 85/2082, and JCSC4744, W.B. Grubb and T. Ito for strain WIS. We also thank D.C. Oliveira for the stimulating discussions about the data described in the manuscript, and C. Milheiriço, N. Faria, and J. Rolo, from the Laboratory of Molecular Genetics, Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa (ITQB/UNL), Oeiras, Portugal, for their help with the PFGE assays.

This work was partially supported by Project CONCORD (Ref. FP7-Health-F3-2008-222718) from the European Community awarded to H. de Lencastre and by grant Ref. 053/BI-BTI/2009 from the same project awarded to O.B. Additional funding was provided by project Tunisia-Portugal MESRST/GRICES ref. Proc° 4.1.5.

The funding agencies had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. No additional external funding was received for this study. The authors have declared that no competing interests exist.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Laboratory of Molecular Genetics, Instituto de Tecnologia Química e Biológica, Oeiras, Portugal

    O. Bouchami, H. de Lencastre & M. Miragaia

  2. Bone Marrow Transplant Centre of Tunisia, Tunis, Tunisia

    O. Bouchami & A. Ben Hassen

  3. Laboratory of Microbiology, The Rockefeller University, New York, NY, USA

    H. de Lencastre

Authors
  1. O. Bouchami
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Ben Hassen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. de Lencastre
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Miragaia
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Miragaia.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bouchami, O., Ben Hassen, A., de Lencastre, H. et al. High prevalence of mec complex C and ccrC is independent of SCCmec type V in Staphylococcus haemolyticus . Eur J Clin Microbiol Infect Dis 31, 605–614 (2012). https://doi.org/10.1007/s10096-011-1354-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-011-1354-3

Keywords

Search

Navigation